Plant-Feeding May Explain Why the Generalist Predator Euseius Stipulatus Does Better on Less Defended Citrus Plants but Tetranyc

Experimental and Applied Acarology (2021) 83:167–182 https://doi.org/10.1007/s10493-020-00588-x Plant‑feeding may explain why the generalist predator Euseius stipulatus does better on less defended citrus plants but Tetranychus‑specialists Neoseiulus californicus and Phytoseiulus persimilis do not Joaquín Cruz‑Miralles1 · Marc Cabedo‑López1 · Michela Guzzo1 · Victoria Ibáñez‑Gual2 · Víctor Flors3 · Josep A. Jaques1 Received: 20 July 2020 / Accepted: 24 December 2020 / Published online: 22 January 2021 © The Author(s) 2021 Abstract The generalist predator Euseius stipulatus (Athias-Henriot) and the Tetranychidae-specialist predators Neoseiulus californicus (McGregor) and Phytoseiulus persimilis Athias-Hen- riot play a key role in the regulation of Tetranychus urticae Koch in Spanish citrus orchards. Previous studies have shown that sour orange (Citrus aurantium L.) and Cleopatra mandarin (Citrus reshni hort. ex Tan.) display extreme resistance and susceptibility to T. urticae, respectively. When ofered a choice between these two genotypes infested by T. urticae, E. stipulatus preferred Cleopatra mandarin, whereas the specialists did not show any preference. The present study was undertaken to check whether these preferences could be related to the feeding of E. stipulatus on the host plant and/or to diferences in prey feeding on the two plants. Our results demonstrate that E. stipulatus is a zoophytophagous mite, which can engage in direct plant feeding in sour orange and Cleopatra mandarin, whereas neither N. californicus nor P. persimilis do so. Whereas Cleopatra mandarin provided a higher-quality prey/feeding substrate for E. stipulatus, which may be related to its phy- tophagy, no diferences were observed for the two specialists. As higher constitutive and faster inducible defense against T. urticae in sour orange relative to Cleopatra mandarin plants result in sour orange supporting lower T. urticae densities and plant damage, our results demonstrate that pest regulation by specialist natural enemies may be more efective when prey feed on better defended plants. Keywords Phytoseiidae · Zoophytophagy · Plant defense · Sour orange · Cleopatra mandarin * Josep A. Jaques [email protected] 1 Departament de Ciències Agràries i del Medi Natural, Universitat Jaume I (UJI), Castelló de la Plana, Spain 2 Departament de Matemàtiques, Universitat Jaume I, UJI, Campus del Riu Sec, 12071 Castelló de la Plana, Spain 3 Integración Metabólica y Señalización Celular, Departament de Ciències Agràries i del Medi Natural, Universitat Jaume I (UJI), Castelló de la Plana, Spain Vol.:(0123456789)1 3 168 Experimental and Applied Acarology (2021) 83:167–182 Introduction Phytoseiid mites (Mesostigmata; Phytoseiidae) have a diversity of lifestyles related to food utilization (McMurtry et al. 2013) ranging from specialized predators of herbivorous spider mites belonging to the genus Tetranychus (Prostigmata: Tetranychidae) (i.e., Phytoseiulus persimilis Athias-Henriot) to omnivorous pollen feeders that also feed on microarthropods and on plant cell-sap (i.e., the genus Euseius). Intermediate diet specializations are com- mon in this family (McMurtry et al. 2013). In Spanish citrus orchards, the herbivore Tet- ranychus urticae Koch, a key pest of clementine mandarins (Pascual Ruiz et al. 2014), and the phytoseiids P. persimilis, Euseius stipulatus (Athias-Henriot) and Neoseiulus californicus (McGregor) coexist. These predators play a key role in the biological control of T. urticae in this agroecosystem (Aguilar-Fenollosa et al. 2011a, b; Pascual Ruiz et al. 2014; Pérez-Sayas et al. 2015). Whereas P. persimilis is a strict entomophagous species, E. stipulatus is a generalist omnivore suspected to feed on plant cell-sap. Neoseiulus californicus can also feed on tetranychid mites and plant-derived food (i.e., pollen) but most probably does not engage in plant cell-sap feeding (Adar et al. 2012; McMurtry and Croft 1997; McMurtry et al. 2013). Cruz-Miralles et al. (2019) showed that E. stipulatus can induce plant defense responses in citrus similar to zoophytophagous predators (Dumont et al. 2018). These authors focused their study on two citrus species: sour orange, Citrus aurantium L., and Cleopatra mandarin, Citrus reshni hort. ex Tan., as they display extreme resistance and susceptibility to T. urticae, respectively (Agut et al. 2014; Bruessow et al. 2010). Sour orange is cultivated worldwide. Its high adaptability to all soil types, which induces good bearing and excellent fruit quality, made sour orange one of the most widely used rootstocks in the citrus industry in the Mediterranean area and in the Americas until the 1950s (Moreno et al. 2008). The emergence of the citrus quick decline disease, caused by the Citrus tristeza virus (CTV, Closteroviridae), killed almost 100 million citrus trees grafted on this rootstock worldwide (Moreno et al. 2008). This forced the massive replacement of sour orange by CTV-tolerant rootstocks, such as Cleopatra mandarin. These tolerant rootstocks, though, are more sus- ceptible to T. urticae than sour orange (Bruessow et al. 2010). Indeed, this massive replacement is considered one of the triggers for the increasing prevalence of T. urticae as a pest of citrus (Bruessow et al. 2010). The diferences in susceptibility to T. urticae between sour orange and Cleopatra mandarin are attributed to a higher constitutive and earlier inducible direct defense related to the oxylipin defensive pathway upon mite attack in sour orange compared to Cleopatra mandarin (Agut et al. 2014, 2015, 2016). These induced genotype- dependent responses closely match those triggered by E. stipulatus (Cruz-Miralles et al. 2019). Together with results by Gómez-Martínez et al. (2020) showing that this phytoseiid is able to obtain liquids by piercing a paraflm membrane, these results could be taken as an indirect evidence of the plant cell-sap feeding of E. stipulatus. Indeed, the cheliceral morphology typical of phytoseiid plant cell-sap feeders has been observed in diferent species of the genus Euseius (Adar et al. 2012). However, attempts to demonstrate feeding of E. stipulatus on leaves of lemon [Citrus limon (L) Burm. f.] and avocado (Persea americana Mill.) failed (Porres et al. 1975). This could be attributed to the plant feeding being cultivar-specifc (Adar et al. 2012). Defnite evidence for plant feeding is therefore needed to relate the observed plant defense responses to presumed herbivory by E. stipulatus (Cruz-Miralles et al. 2019). Contrary to E. stipulatus, N. californicus is suspected not to feed on plant cell sap based on its cheliceral traits (Adar et al. 2012; McMurtry et al. 2013). Phytoseiulus persimilis, 1 3 Experimental and Applied Acarology (2021) 83:167–182 169 the third phytoseiid in the system, does not feed on plants (Magalhães and Bakker 2002; McMurtry and Croft 1997; McMurtry et al. 2013; Nomikou et al. 2003). These diet specializations could explain the responses of these phytoseiids when ofered a choice between T. urticae-infested sour orange and Cleopatra mandarin plants Cabedo-López et al. (2019). Although a preference for less defended plants (i.e., infested Cleopatra mandarin rather than infested sour orange) was anticipated (keep in mind that prey densities should be higher on these plants), only E. stipulatus behaved as expected, whereas the other two phytoseiids showed no preference (Cabedo-López et al. (2019). This could be explained by the presumed herbivory of E. stipulatus, which would make this phytoseiid beneft from feeding directly on the less defended plant (Cleopatra mandarin) in periods when prey are scarce. This would not apply to the other two phytoseiids. Moreover, as there is evidence that fecundity of P. persimilis can double depending on the plant on which its prey, T. urticae, are feeding (Popov and Khudyakova 1989), we wondered whether prey proftability on sour orange and Cleopatra mandarin would be the same for these predators. To challenge the hypotheses that (1) E. stipulatus is a zoophytophagous mite engaging in direct plant feeding and that (2) T. urticae proftability for the three phytoseiids considered is independent of the prey feeding substrate (sour orange and Cleopatra mandarin), we performed two experiments. In the frst, we characterized leaf cuticular damage on sour orange and Cleopatra mandarin plants after exposure to T. urticae (positive control) and to each of the three phytoseiid species. In the second experiment, we evaluated prey and phytoseiid population growth (as a proxy of plant and prey proftability) on T. urticae-infested sour orange and Cleopatra mandarin plants. These results should help us to better under- stand direct and prey-mediated efects of plants on predators, and could provide clues for a more sustainable management of T. urticae. Materials and methods Mite rearing and all experiments were carried out at controlled environmental conditions of 22 ± 5 °C; 60 ± 10% RH and 16:8 h L:D photoperiod with an illuminance of 5000 lx. Plant material Three-month-old plants of sour orange and Cleopatra mandarin (with 10–12 true fully developed leaves) were used in our assays. They were obtained from seeds collected in trees cultivated at UJI campus and grown on vermiculite and peat (1:3; vol:vol) in 320-ml pots in a climatic chamber. To prevent any host-related maternal efect that could difer- entially afect the ftness of the mites used in our assays (Marshall and Uller 2007), mite stock colonies were maintained on either pesticide-free lemons [Citrus limon (L.) Burm f.], or bean plants (Phaseolus vulgaris L. cv. Buenos Aires Roja). These were also produced at UJI campus. Typha sp. pollen collected nearby was used to maintain phytoseiid stock colonies. Spider mite stock colony The colony of T. urticae used in our assays, was initiated with specimens originally collected in 2001 in clementine orchards near UJI campus. Spider mites were maintained on lemons in a climatic chamber following Cruz-Miralles et al. (2019). In short, 8–10 lemons 1 3 170 Experimental and Applied Acarology (2021) 83:167–182 were set on top of a wooden structure placed in an open plastic box (40 × 30 × 8 cm) half- flled with water.

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